Cited by 136Oral microbiology and periodontitis researchBacterial biofilms and quorum sensingBacterial Genetics and Biotechnology

Dynamics of Streptococcus mutans Transcriptome in Response to Starch and Sucrose during Biofilm Development

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Klein, Marlise I., DeBaz, Lena, Agidi, Senyo, Lee, Herbert, Xie, Gary, Lin, Amy H.-M., Hamaker, Bruce R., Lemos, José A. +1 more·2010·PLoS ONE

Abstract

The combination of sucrose and starch in the presence of surface-adsorbed salivary α-amylase and bacterial glucosyltransferases increase the formation of a structurally and metabolically distinctive biofilm by Streptococcus mutans. This host-pathogen-diet interaction may modulate the formation of pathogenic biofilms related to dental caries disease. We conducted a comprehensive study to further investigate the influence of the dietary carbohydrates on S. mutans-transcriptome at distinct stages of biofilm development using whole genomic profiling with a new computational tool (MDV) for data mining. S. mutans UA159 biofilms were formed on amylase-active saliva coated hydroxyapatite discs in the presence of various concentrations of sucrose alone (ranging from 0.25 to 5% w/v) or in combination with starch (0.5 to 1% w/v). Overall, the presence of sucrose and starch (suc+st) influenced the dynamics of S. mutans transcriptome (vs. sucrose alone), which may be associated with gradual digestion of starch by surface-adsorbed amylase. At 21 h of biofilm formation, most of the differentially expressed genes were related to sugar metabolism, such as upregulation of genes involved in maltose/maltotriose uptake and glycogen synthesis. In addition, the groEL/groES chaperones were induced in the suc+st-biofilm, indicating that presence of starch hydrolysates may cause environmental stress. In contrast, at 30 h of biofilm development, multiple genes associated with sugar uptake/transport (e.g. maltose), two-component systems, fermentation/glycolysis and iron transport were differentially expressed in suc+st-biofilms (vs. sucrose-biofilms). Interestingly, lytT (bacteria autolysis) was upregulated, which was correlated with presence of extracellular DNA in the matrix of suc+st-biofilms. Specific genes related to carbohydrate uptake and glycogen metabolism were detected in suc+st-biofilms in more than one time point, indicating an association between presence of starch hydrolysates and intracellular polysaccharide storage. Our data show complex remodeling of S. mutans-transcriptome in response to changing environmental conditions in situ, which could modulate the dynamics of biofilm development and pathogenicity.

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  1. [45]Tanzer JM Freedman ML Woodiel FN Eifert RL Rinehimer LA 1976 Association of Streptococcus mutans virulence with synthesis of intracellular polysaccharide.. Stiles HM Loesche WJ O'Brien TL Special supplement to Microbiology Abstracts London Information Retrieval, Inc 596 616 In: Proceedings in microbiology. Aspects of dental caries

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Authors
Klein, M. I., DeBaz, L., Agidi, S., Lee, H., Xie, G., Lin, A. H.-M., Hamaker, B. R., Lemos, J. A., & Koo, H.
Affiliations
  • University of Rochester Medicine (US)
  • Los Alamos National Laboratory (US)
  • Purdue University West Lafayette (US)
Corresponding author
Koo, Hyun
Venue
PLoS ONE
Published
2010-10-19
Volume
5
Issue
10
Pages
e13478
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2141894926
Cited by
136
References
53
Citations by year
2026: 1 · 2025: 7 · 2024: 5 · 2023: 9 · 2022: 9 · 2021: 12 · 2020: 8 · 2019: 8 · 2018: 2 · 2017: 10 · 2016: 9 · 2015: 10 · 2014: 11 · 2013: 13 · 2012: 13
FWCI
12.98
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Purdue e-Pubs (Purdue University System) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
Funders
  • National Institutes of Health
  • Office of the President, University of California
  • National Institute of Dental and Craniofacial Research (Y01 DE006006, Y1-DE-6006-02)
Topics
  • Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
Streptococcus mutans, biofilm growth, transcriptome dynamics, starch, sucrose, salivary amylase, glucosyltransferase, dental caries, carbohydrate metabolism, glycogen synthesis, extracellular DNA, polysaccharide storage, gene expression profiling
MeSH terms
Base Sequence, Genes, Bacterial, Starch, Streptococcus mutans, Sucrose, DNA Primers, Biofilms, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling

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